Vol. 499: 193–201, 2014 MARINE ECOLOGY PROGRESS SERIES Published March 3 doi: 10.3354/meps10637 Mar Ecol Prog Ser Genetic structure among spawning aggregations of the gulf coney Hyporthodus acanthistius Ricardo Beldade1,2,3,4,*, Alexis M. Jackson1, Richard Cudney-Bueno5,6, Peter T. Raimondi1, Giacomo Bernardi1 1Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 100 Shaffer Road, Santa Cruz, California 95060, USA 2USR 3278 CRIOBE, CNRS EPHE, CBETM de l’Université de Perpignan, 66860 Perpignan Cedex, France 3Laboratoire d’excellence ‘Corail’, USR 3278 CRIOBE CNRS-EPHE, 66860 Perpignan Cedex, France 4Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal 5School of Natural Resources and the Environment, University of Arizona, Biological Sciences East, Room 325, Tucson, Arizona 85721, USA 6Institute of Marine Sciences, University of California Santa Cruz, 100 Shaffer Road, Santa Cruz, California 95060, USA ABSTRACT: Many large groupers form spawning aggregations, returning to the same spawning sites in consecutive spawning seasons. Connectivity between spawning aggregations is thus assured by larval dispersal. This study looks into the genetic structure and gene flow among spawning aggregations of a large grouper, the gulf coney Hyporthodus acanthistius, in the north- ern Gulf of California. First, using the mitochondrial control region and 11 microsatellites, we cal- culated FST metrics and conducted a Bayesian clustering analysis to determine structure among 5 spawning aggregations. Shallow genetic structure was found, separating the southernmost spawning aggregate from the remainder. Second, we used the results from the structure analysis and local water circulation patterns to delineate 3 distinct models of gene flow. The best-sup- ported model, in which the southernmost spawning aggregate formed one group and all other spawning aggregates were nested into a second group, was the one that was consistent with water circulation during the species’ spawning season. Larval retention within a seasonal anti - cyclonic gyre that formed during the gulf coney’s spawning season may be responsible for the pat- terns found. This study highlights the importance of local oceanographic conditions in dictating the structure among spawning aggregations even at small geographic scales and contributes to informed management plans for this overexploited grouper. KEY WORDS: Grouper · Dispersal · Connectivity · Sea of Cortez · Oceanography · Eddies · Retention · Migration models · Rooster hind · Epinephelus Resale or republication not permitted without written consent of the publisher INTRODUCTION cal populations via the dispersal of larvae, juveniles or adults (Sale et al. 2005), which influences almost Knowledge of how genetic variation is partitioned all ecological and evolutionary processes in meta - in the ocean is fundamental for understanding the populations (Hanski & Gaggiotti 2004). Genetic ecology, conservation and management of marine connectivity has been shown across a range of geo- resources (Mora & Sale 2002, Gell & Roberts 2003, graphical scales among different marine taxa, ranging Cowen et al. 2007, Francis et al. 2007, Planes et from virtually panmictic throughout considerably al. 2009). One of the strongest drivers of genetic struc- large geographic ranges (Bowen et al. 2001, Lessios et ture is connectivity, i.e. the demographic linking of lo- al. 2003, Klanten et al. 2007, Beldade et al. 2009, Leray *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 194 Mar Ecol Prog Ser 499: 193–201, 2014 et al. 2010) to clearly structured populations at very The northern Gulf of California (NGC) is home to small scales (Sotka et al. 2004, Bernardi 2005, Barber several fishes that aggregate to spawn and is part of et al. 2006, Gerlach et al. 2007, Beldade et al. 2012). one of the most productive marine ecosystems in Many fish form spawning aggregations (i.e. groups the world, contributing most of Mexico’s fishery re - of conspecific fish that gather for the purpose of sources (Arvizu-Martínez 1987, Lluch-Cota et al. spawning, with densities or numbers significantly 2007, Erisman et al. 2012). The NGC covers a rela- higher than those found in the area of aggregation tively small area extending from the Colorado delta during non-reproductive periods; Domeier & Colin in the north to Bahia de Los Angeles and Isla Tiburon 1997), including groupers, snappers, jacks, surgeon- in the south (Fig. 1). In this region, in-depth know- fishes, damselfishes and parrotfishes (Sala et al. ledge of water circulation patterns and other geomor- 2003, Erisman et al. 2007, Gladstone 2007, Sadovy phological characteristics (Fig. 1) provide a unique de Mitcheson et al. 2008, Gerhardinger et al. 2009). opportunity to describe genetic structure and test Some groupers return to the same spawning sites in models of gene flow in locally occurring species. In consecutive spawning seasons (Sala et al. 2001, Starr the NGC, the main oceanographic features comprise et al. 2007), in some cases covering large distances intense tidal mixing (Argote et al. 1995) and a sea- to do so (Bolden 2000). If adult spawning aggrega- sonally reversing gyre, anticyclonic in summer (June tion site fidelity is indeed ubiquitous among large to September) (Fig. 1B) and cyclonic in winter groupers, then the dispersal of the pelagic larval (Fig. 1C) (Lavín et al. 1997, Marinone et al. 2008); stages that are subjected to transport by ocean cur- strong coastal currents along the eastern Sonora rents should be the main driver of genetic connec - coastline (Peguero-Icaza et al. 2011); and small resid- tivity. Two elements underline the importance of ual currents and small eddies in the upper gulf (Mari- oceanographic characteristics to the dispersal of none et al. 2011). These characteristics are likely to spawning aggregation offspring. First, the specific influence the transport of larvae in the NGC (Mari- location of spawning aggregations appears to maxi- none et al. 2004, Cudney-Bueno et al. 2009). Both mize the rapid advection of eggs and larvae away local water circulation and bottom geomorphologic from the reef environment (e.g. Choat 2012, Colin characteristics may have important implications for 2012a). Second, knowledge of the onset of sensorial the formation of spawning aggregations as well as for and swimming abilities of pelagic larvae, which in the fate of eggs or larvae released there (Cherubin et the case of groupers is still largely unknown, is al. 2011, Karnauskas et al. 2011). In the NGC, there essential to understand how larval abilities might are 2 deep basins, the Delfin Basin (800 m) and the steer the dispersal process (e.g. Colin 2012b, Hamner Wagner Basin (200 m), and several sills (Lavín et al. & Largier 2012). Larval abundance and even the 1997) whose putative part in limiting dispersal of lar- magnitude of recruitment events appear to be corre- vae or concentrating prey for early larval stages lated with oceanographic and climatic parameters, remains unclear (e.g. Karnauskas et al. 2011). such as temperature, salinity and depth (but see e.g. The gulf coney Hyporthodus acanthistius (formerly Aburto-Oropeza et al. 2010, Marancik et al. 2012). Epinephelus acanthistius; Craig & Hastings 2007) is a Fig. 1. Northern Gulf of California (NGC) including (A) bathymetry (depth in meters) and named sampled spawning aggrega- tions of the gulf coney Hyporthodus acanthistius (PLI, Puerto Libertad; PLO, Puerto Lobos; STO, Santo Tomas; PPE, Puerto Peñasco; and SLG, San Luiz Gonzaga); (B) ocean circulation in the summer (only the month of July is represented); and (C) in the winter (only the month of January is represented). Ocean circulation reproduced from Marinone (2003) by permission of the American Geophysical Union Beldade et al.: Genetic structure among grouper spawning aggregations 195 tropical and subtropical large grouper that occurs sulfate) overnight at 55°C. This was followed by from southern California to Peru (Heemstra & Ran- purification using phenol/chloroform ex tractions and dall 1993), including the Gulf of California (or Sea of alcohol precipitation (Sambrook et al. 1989). Cortez) (Cudney-Bueno & Turk-Boyer 1998, Aburto- Oropeza et al. 2008). It is found at depths greater than ~45 m usually in silty areas adjacent to rocky mtDNA and microsatellites reefs (Thomson et al. 2000), and spawns in aggre- gations on muddy bottoms during the spring and We amplified the 5’ end of the hyper-variable por- summer months (Cudney-Bueno & Turk-Boyer 1998). tion of the mitochondrial control region using the During the spawning period, artisanal fishermen universal primers CR-A and CR-E (Lee et al. 1995). heavily target this species (Aburto-Oropeza et al. Each 100 µl reaction contained 10 to 100 ng of DNA, 2008). Indeed, the high commercial value and tempo- 10 mM Tris HCl (pH 8.3), 50 mM KCl, 1.5 mM MgCl2, ral and spatial predictability of their mass gatherings 2.5 units of Taq DNA polymerase (Perkin-Elmer), make groupers a prime target for fisheries. Despite 150 mM of each dNTP, and 0.3 mM of each primer its present ‘Least Concern’ conservation status (IUCN and was amplified with a cycling profile of 45 s at 2012), the abundance of the gulf coney in the NGC 94°C, 1 min at 52°C and 1 min at 72°C for 35 cycles. has been rapidly declining over the past 2 decades After purification of amplified DNA genes following (Aburto-Oropeza et al. 2008). Elsewhere, there are the manufacturer’s protocol (ABI, Perkin-Elmer), we many examples of collapsed grouper spawning sequenced on an ABI 3100 automated sequencer aggregations because of overfishing such as the Nas- (Applied Biosystems). sau grouper E. striatus (e.g. Sala et al. 2001, Aguilar- All individuals were genotyped for 13 microsatel- Perera 2006) and the gulf grouper Mycteroperca jor- lites following protocols described in Molecular Eco - dani (Sáenz-Arroyo et al. 2005). Given the threat of logy Resources Primer Development Consortium et overfishing to fish that form spawning aggregations al. (2009). Each individual was genotyped using (Sadovy de Mitcheson et al.